Developmentally programmed cell death in Drosophila
Open accessAbstract
During the development of metazoans, programmed cell death (PCD) is essential for tissue patterning, removal of unwanted cells and maintaining homeostasis. In the past 20 years Drosophila melanogaster has been one of the systems of choice for studies involving developmental cell death, providing an ideal genetically tractable model of intermediary complexity between Caenorhabditis elegans and mammals. The lessons learned from studies using Drosophila indicate both the conserved nature of the many cell death pathways as well as novel and unexpected mechanisms. In this article we review the understanding of PCD during Drosophila development, highlighting the key mechanisms that are evolutionarily conserved as well as apparently unusual pathways, which indicate divergence, but provide evidence of complexity acquired during organismic evolution. This article is part of a Special Section entitled: Cell Death Pathways.
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The major players of the apoptotic pathway are largely conserved between mammals and Drosophila and C. elegans.
“The details of the apoptotic pathway differ between mammals and the model organisms Drosophila and C. elegans, however the major players are largely conserved (Figure 1).”
From Programmed cell death in aging (2015) · cites this paper as Denton et al., 2013
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Apoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics
Kerr, J. F. R., Wyllie, A. H., & Currie, A. R. (1972) · British Journal of Cancer · doi:10.1038/bjc.1972.33 · Cited by 15,673 · see citing works
The Bcl-2 Protein Family: Arbiters of Cell Survival
Adams, J. M., & Cory, S. (1998) · Science · doi:10.1126/science.281.5381.1322 · Cited by 5,303 · see citing works
Ji, Y. (1993) · Cell · doi:10.1016/0092-8674(93)90485-9 · Cited by 2,497 · see citing works
Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.96 · Cited by 2,421 · see citing works
Self-citationEaten alive: a history of macroautophagy
Yang, Z., & Klionsky, D. J. (2010) · Nature Cell Biology · doi:10.1038/ncb0910-814 · Cited by 2,096 · see citing works
Genetic control of programmed cell death in the nematode C. elegans
Ellis, H. (1986) · Cell · doi:10.1016/0092-8674(86)90004-8 · Cited by 1,828 · see citing works
An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif
Crook, N. E., Clem, R. J., & Miller, L. K. (1993) · Journal of Virology · doi:10.1128/jvi.67.4.2168-2174.1993 · Cited by 1,058 · see citing works
Genetic Control of Programmed Cell Death in Drosophila
White, K., Grether, M. E., Abrams, J., Young, L. M., Farrell, K., & Steller, H. (1994) · Science · doi:10.1126/science.8171319 · Cited by 1,047 · see citing works
Caenorhabditis elegans gene ced-9 protects cells from programmed cell death
Hengartner, M. O., Ellis, R. E., & Horvitz, H. R. (1992) · Nature · doi:10.1038/356494a0 · Cited by 889 · see citing works
Life in the balance: how BH3-only proteins induce apoptosis
Willis, S. N., & Adams, J. M. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.10.001 · Cited by 743 · see citing works
Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation
Yao, T., Segraves, W. A., Oro, A. E., McKeown, M., & Evans, R. M. (1992) · Cell · doi:10.1016/0092-8674(92)90266-f · Cited by 716 · see citing works
Programmed cell death during Drosophila embryogenesis
Abrams, J., White, K., Fessler, L. I., & Steller, H. (1993) · Development · doi:10.1242/dev.117.1.29 · Cited by 710 · see citing works
The head involution defective gene of Drosophila melanogaster functions in programmed cell death.Preprint
Grether, M. E., Abrams, J., Agapite, J., White, K., & Steller, H. (1995) · Genes & Development · doi:10.1101/gad.9.14.1694 · Cited by 700 · see citing works
Conradt, B., & Horvitz, H. R. (1998) · Cell · doi:10.1016/s0092-8674(00)81182-4 · Cited by 642 · see citing works
IAPs, RINGs and ubiquitylation
Vaux, D. L., & Silke, J. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1621 · Cited by 611 · see citing works
Growth Arrest and Autophagy Are Required for Salivary Gland Cell Degradation in Drosophila
Berry, D. L., & Baehrecke, E. H. (2007) · Cell · doi:10.1016/j.cell.2007.10.048 · Cited by 602 · see citing works
Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle
Thomas, H. E., Stunnenberg, H. G., & Stewart, A. F. (1993) · Nature · doi:10.1038/362471a0 · Cited by 520 · see citing works
Wang, S. L., Hawkins, C. J., Yoo, S. J., Müller, H. ‐. J., & Hay, B. A. (1999) · Cell · doi:10.1016/s0092-8674(00)81974-1 · Cited by 505 · see citing works
Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway
Igaki, T., Kanda, H., Yamamoto‐Goto, Y., Kanuka, H., Kuranaga, E., Aigaki, T., & Miura, M. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf306 · Cited by 462 · see citing works
The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers.
DiBello, P. R., Withers, D. A., Bayer, C. A., Fristrom, J. W., & Guild, G. M. (1991) · Genetics · doi:10.1093/genetics/129.2.385 · Cited by 447 · see citing works
The emergence of order in the Drosophila pupal retina
Cagan, R. L., & Ready, D. F. (1989) · Developmental Biology · doi:10.1016/0012-1606(89)90261-3 · Cited by 443 · see citing works
grim, a novel cell death gene in Drosophila.Preprint
Chen, P., Nordstrom, W., Gish, B., & Abrams, J. (1996) · Genes & Development · doi:10.1101/gad.10.14.1773 · Cited by 428 · see citing works
Caspase Activity and a Specific Cytochrome C Are Required for Sperm Differentiation in Drosophila
Arama, E., Agapite, J., & Steller, H. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00120-5 · Cited by 417 · see citing works
The Drosophila caspase Dredd is required to resist Gram‐negative bacterial infection
Leulier, F., Rodríguez, A., Khush, R. S., Abrams, J., & Lemaître, B. (2000) · EMBO Reports · doi:10.1093/embo-reports/kvd073 · Cited by 411 · see citing works
Burtis, K. C., Thummel, C. S., Jones, C. W., Karim, F. D., & Hogness, D. S. (1990) · Cell · doi:10.1016/0092-8674(90)90217-3 · Cited by 409 · see citing works
Yuan, J., & Horvitz, H. R. (1992) · Development · doi:10.1242/dev.116.2.309 · Cited by 403 · see citing works
How death shapes life during development
Baehrecke, E. H. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm931 · Cited by 402 · see citing works
Steroid regulated programmed cell death during Drosophila metamorphosis
Jiang, C., Baehrecke, E. H., & Thummel, C. S. (1997) · Development · doi:10.1242/dev.124.22.4673 · Cited by 392 · see citing works
Autophagy, Not Apoptosis, Is Essential for Midgut Cell Death in Drosophila
Denton, D., Shravage, B., Simin, R., Mills, K., Berry, D. L., Baehrecke, E. H., & Kumar, S. (2009) · Current Biology · doi:10.1016/j.cub.2009.08.042 · Cited by 385 · see citing works
Self-citationCell death by autophagy: facts and apparent artefacts
Denton, D., Nicolson, S., & Kumar, S. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.146 · Cited by 381 · see citing works
Self-citationHid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms
Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L., Feldman, R. M. R., Clem, R. J., Müller, H. ‐. J., & Hay, B. A. (2002) · Nature Cell Biology · doi:10.1038/ncb793 · Cited by 373 · see citing works
Cell death in normal and rough eye mutants of Drosophila
Wolff, T., & Ready, D. F. (1991) · Development · doi:10.1242/dev.113.3.825 · Cited by 372 · see citing works
Evolution of TNF Signaling Mechanisms
Moreno, E., Yan, M., & Basler, K. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00954-5 · Cited by 360 · see citing works
Caspase-mediated processing of the Drosophila NF-κB factor Relish
Stöven, S., Silverman, N. S., Junell, A., Hedengren-Olcott, M., Erturk, D., Engström, Y., Maniatis, T., & Hultmark, D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1035902100 · Cited by 351 · see citing works
Activation of the Drosophila NF‐κB factor Relish by rapid endoproteolytic cleavage
Stöven, S., Andó, I., Kadalayil, L., Engström, Y., & Hultmark, D. (2000) · EMBO Reports · doi:10.1093/embo-reports/kvd072 · Cited by 339 · see citing works
DCP-1, a Drosophila Cell Death Protease Essential for Development
Song, Z., McCall, K., & Steller, H. (1997) · Science · doi:10.1126/science.275.5299.536 · Cited by 337 · see citing works
The Drosophila caspase DRONC is regulated by DIAP1
Meier, P., Silke, J., Leevers, S. J., & Evan, G. I. (2000) · The EMBO Journal · doi:10.1093/emboj/19.4.598 · Cited by 333 · see citing works
Rodriguez, A., Oliver, H., Zou, H., Chen, P., Wang, X., & Abrams, J. (1999) · Nature Cell Biology · doi:10.1038/12984 · Cited by 332 · see citing works
CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis
Inohara, N., Koseki, T., Hu, Y., Chen, S., & Núñez, G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10717 · Cited by 315 · see citing works
The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis
Wilson, R., Goyal, L., Ditzel, M., Zachariou, A., Baker, D. A., Agapite, J., Steller, H., & Meier, P. (2002) · Nature Cell Biology · doi:10.1038/ncb799 · Cited by 296 · see citing works
DRONC, an ecdysone-inducible Drosophila caspase
Dorstyn, L., Colussi, P. A., Quinn, L. M., Richardson, H. E., & Kumar, S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4307 · Cited by 283 · see citing works
Self-citationRegulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1
Ryoo, H. D., Bergmann, A., Gonen, H., Ciechanover, A. J., & Steller, H. (2002) · Nature Cell Biology · doi:10.1038/ncb795 · Cited by 278 · see citing works
Jiang, C., Lamblin, A.-F., Steller, H., & Thummel, C. S. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80439-6 · Cited by 270 · see citing works
Essential Role of CED-4 Oligomerization in CED-3 Activation and Apoptosis
Yang, X., Chang, H. Y., & Baltimore, D. (1998) · Science · doi:10.1126/science.281.5381.1355 · Cited by 269 · see citing works
Spatial and temporal patterns of E74 transcription during Drosophila development
Thummel, C. S., Burtis, K. C., & Hogness, D. S. (1990) · Cell · doi:10.1016/0092-8674(90)90218-4 · Cited by 262 · see citing works
Nezis, I. P., Shravage, B. V., Sagona, A. P., Lamark, T., Bjørkøy, G., Johansen, T., Rusten, T. E., Brech, A., Baehrecke, E. H., & Stenmark, H. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201002035 · Cited by 252 · see citing works
Inhibitor of apoptosis 2 and TAK1‐binding protein are components of the Drosophila Imd pathway
Kleino, A., Valanne, S., Ulvila, J., Kallio, J., Myllymäki, H., Enwald, H., Stöven, S., Poidevin, M., Ueda, R., Hultmark, D., et al. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600807 · Cited by 246 · see citing works
Broadus, J., McCabe, J. R., Endrizzi, B. T., et al. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80305-6 · Cited by 245 · see citing works
Control of the Cell Death Pathway by Dapaf-1, a Drosophila Apaf-1/CED-4-Related Caspase Activator
Kanuka, H., Sawamoto, K., Inohara, N., Matsuno, K., Okano, H., & Miura, M. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80386-x · Cited by 236 · see citing works
Dredd,a Novel Effector of the Apoptosis ActivatorsReaper, Grim,andHidinDrosophila
Chen, P., Rodriguez, A., Erskine, R., Thach, T., & Abrams, J. (1998) · Developmental Biology · doi:10.1006/dbio.1998.9000 · Cited by 232 · see citing works
Hawkins, C. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000869200 · Cited by 224 · see citing works
Genome-Wide Analyses of Steroid- and Radiation-Triggered Programmed Cell Death in Drosophila
Lee, C.-Y., Clough, E. A., Yellon, P., Teslovich, T. M., Stephan, D. A., & Baehrecke, E. H. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00085-x · Cited by 215 · see citing works
Steroid Regulation of Midgut Cell Death during Drosophila Development
Lee, C.-Y., Cooksey, B. A. K., & Baehrecke, E. H. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0784 · Cited by 214 · see citing works
A SAGE Approach to Discovery of Genes Involved in Autophagic Cell Death
Gorski, S. M., Chittaranjan, S., Pleasance, E. D., Freeman, J. D., Anderson, C. L., Varhol, R. J., Coughlin, S. M., Zuyderduyn, S. D., Jones, S. J. M., & Marra, M. A. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00082-4 · Cited by 213 · see citing works
Hawkins, C. J., Yoo, S. J., Peterson, E. P., Wang, S. L., Vernooy, S. Y., & Hay, B. A. (2000) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)61483-3 · Cited by 203 · see citing works
Identification of a Drosophila melanogaster ICE/CED‐3‐related protease, drICE
Fraser, A. G., & Evan, G. I. (1997) · The EMBO Journal · doi:10.1093/emboj/16.10.2805 · Cited by 201 · see citing works
The Jekyll and Hyde Functions of Caspases
Yi, C. H., & Yuan, J. (2009) · Developmental Cell · doi:10.1016/j.devcel.2008.12.012 · Cited by 198 · see citing works
Zhou, L., Song, Z., Tittel, J. N., & Steller, H. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80385-8 · Cited by 196 · see citing works
DRONC Coordinates Cell Death and Compensatory Proliferation
Kondo, S., Senoo‐Matsuda, N., Hiromi, Y., & Miura, M. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00183-06 · Cited by 194 · see citing works
Kanda, H., Igaki, T., Kanuka, H., Yagi, T., & Miura, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200324200 · Cited by 190 · see citing works
E93 Directs Steroid-Triggered Programmed Cell Death in Drosophila
Lee, C., Wendel, D. P., Reid, P. W., Lam, G., Thummel, C. S., & Baehrecke, E. H. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00042-3 · Cited by 188 · see citing works
Xu, D., Li, Y., Arcaro, M. J., Lackey, M., & Bergmann, A. (2005) · Development · doi:10.1242/dev.01790 · Cited by 182 · see citing works
Huh, J. R., Vernooy, S. Y., Yu, H., Yan, N., Shi, Y., Guo, M., & Hay, B. A. (2003) · PLoS Biology · doi:10.1371/journal.pbio.0020015 · Cited by 181 · see citing works
Hou, Y.-C. C., Chittaranjan, S., Barbosa, S. G., McCall, K., & Gorski, S. M. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200712091 · Cited by 180 · see citing works
Colussi, P. A., Quinn, L. M., Huang, D. C. S., et al. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.148.4.703 · Cited by 179 · see citing works
Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency
Foley, K. M., & Cooley, L. (1998) · Development · doi:10.1242/dev.125.6.1075 · Cited by 173 · see citing works
Daish, T. J., Mills, K., & Kumar, S. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.09.018 · Cited by 171 · see citing works
Self-citationMuro, I., Hay, B. A., & Clem, R. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203464200 · Cited by 170 · see citing works
Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila
Kauppila, S., Maaty, W. S. A., Chen, P., Tomar, R. S., Eby, M. T., Chapo, J., Chew, S.-K., Rathore, N., Zachariah, S., Sinha, S. K., et al. (2003) · Oncogene · doi:10.1038/sj.onc.1206715 · Cited by 166 · see citing works
Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis
Barth, J. M. I., Szabad, J., Hafen, E., & Köhler, K. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.157 · Cited by 165 · see citing works
Kumar, S., & Doumanis, J. (2000) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400756 · Cited by 165 · see citing works
Self-citationBaehrecke, E. H., & Thummel, C. S. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1262 · Cited by 165 · see citing works
An Essential Role for the Caspase Dronc in Developmentally Programmed Cell Death in Drosophila
Quinn, L. M., Dorstyn, L., Mills, K., Colussi, P. A., Chen, P., Coombe, M., Abrams, J., Kumar, S., & Richardson, H. E. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002935200 · Cited by 161 · see citing works
Self-citationBuffy, a Drosophila Bcl‐2 protein, has anti‐apoptotic and cell cycle inhibitory functions
Quinn, L. M., Coombe, M., Mills, K., Daish, T., Colussi, P., Kumar, S., & Richardson, H. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg355 · Cited by 157 · see citing works
Self-citationDrob-1, a Drosophila member of the Bcl-2/CED-9 family that promotes cell death
Igaki, T., Kanuka, H., Inohara, N., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.2.662 · Cited by 157 · see citing works
The Apical Caspase dronc Governs Programmed and Unprogrammed Cell Death in Drosophila
Chew, S. K., Akdemir, F., Chen, P., Lu, W.-J., Mills, K., Daish, T., Kumar, S., Rodriguez, A., & Abrams, J. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.09.016 · Cited by 153 · see citing works
Self-citationMuro, I., Berry, D. L., Huh, J. R., Chen, C., Huang, H., Yoo, S. J., Guo, M., Baehrecke, E. H., & Hay, B. A. (2006) · Development · doi:10.1242/dev.02495 · Cited by 150 · see citing works
Molecular mechanism of Reaper-Grim-Hid-mediated suppression of DIAP1-dependent Dronc ubiquitination
Chai, J., Yan, N., Huh, J. R., Wu, J., Li, W., Hay, B. A., & Shi, Y. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb989 · Cited by 149 · see citing works
dFADD, a Novel Death Domain-containing Adapter Protein for theDrosophila Caspase DREDD
Hu, S., & Yang, X. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.c000341200 · Cited by 137 · see citing works
Leulier, F., Lhocine, N., Lemaître, B., & Meier, P. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00548-06 · Cited by 136 · see citing works
A Ubiquitin Ligase Complex Regulates Caspase Activation During Sperm Differentiation in Drosophila
Arama, E., Bader, M., Rieckhof, G. E., & Steller, H. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050251 · Cited by 135 · see citing works
Three-dimensional Structure of a Double Apoptosome Formed by the Drosophila Apaf-1 Related Killer
Yu, X., Wang, L., Acehan, D., Wang, X., & Akey, C. W. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.10.040 · Cited by 134 · see citing works
Gesellchen, V., Kuttenkeuler, D., Steckel, M., Pelte, N., & Boutros, M. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400530 · Cited by 132 · see citing works
Cell death during<i>Drosophila melanogaster</i>early oogenesis is mediated through autophagy
Nezis, I. P., Lamark, T., Velentzas, A. D., Rusten, T. E., Bjørkøy, G., Johansen, T., Papassideri, I. S., Stravopodis, D. J., Margaritis, L. H., Stenmark, H., et al. (2009) · Autophagy · doi:10.4161/auto.5.3.7454 · Cited by 132 · see citing works
Srinivasula, S. M., Datta, P., Kobayashi, M., Wu, J.-W., Fujioka, M., Hegde, R. P., Zhang, Z., Mukattash, R., Fernandes‐Alnemri, T., Shi, Y., et al. (2002) · Current Biology · doi:10.1016/s0960-9822(01)00657-1 · Cited by 131 · see citing works
Dorstyn, L., Mills, K., Lazebnik, Y. A., & Kumar, S. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200408054 · Cited by 128 · see citing works
Self-citationInactivation of Effector Caspases through Nondegradative Polyubiquitylation
Ditzel, M., Broemer, M., Tenev, T., Bolduc, C., Lee, T. V., Rigbolt, K. T. G., Elliott, R. J. R., Zvelebil, M., Blagoev, B., Bergmann, A., et al. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.09.025 · Cited by 128 · see citing works
Xu, D., Wang, Y., Willecke, R., Chen, Z., Ding, T., & Bergmann, A. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401920 · Cited by 128 · see citing works
Christich, A., Kauppila, S., Chen, P., Sogame, N., Ho, S. I., & Abrams, J. (2002) · Current Biology · doi:10.1016/s0960-9822(01)00658-3 · Cited by 125 · see citing works
The two Drosophila cytochrome C proteins can function in both respiration and caspase activation
Arama, E., Bader, M., Srivastava, M., Bergmann, A., & Steller, H. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600920 · Cited by 125 · see citing works
Stage-specific apoptotic patterns during Drosophila oogenesis
Nezis, I. P., Stravopodis, D. J., Papassideri, I. S., Robert‐Nicoud, M., & Margaritis, L. H. (2000) · European Journal of Cell Biology · doi:10.1078/0171-9335-00088 · Cited by 124 · see citing works
DECAY, a Novel Drosophila Caspase Related to Mammalian Caspase-3 and Caspase-7
Dorstyn, L., Read, S. H., Quinn, L. M., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.43.30778 · Cited by 124 · see citing works
The Drosophila Bcl-2 family member dBorg-1 functions in the apoptotic response to UV-irradiation
Brachmann, C. B., Jassim, O. W., Wachsmuth, B. D., et al. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00474-7 · Cited by 123 · see citing works
Eggs to die for: cell death during Drosophila oogenesis
Buszczak, M., & Cooley, L. (2000) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400755 · Cited by 122 · see citing works
Morgue mediates apoptosis in the Drosophila melanogaster retina by promoting degradation of DIAP1
Hays, R., Wickline, L., & Cagan, R. L. (2002) · Nature Cell Biology · doi:10.1038/ncb794 · Cited by 121 · see citing works
Yacobi-Sharon, K., Namdar, Y., & Arama, E. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.02.002 · Cited by 119 · see citing works
Cracking open cell death in the Drosophila ovary
Pritchett, T. L., Tanner, E. A., & McCall, K. (2009) · APOPTOSIS · doi:10.1007/s10495-009-0369-z · Cited by 119 · see citing works
Drosophila sickle Is a Novel grim-reaper Cell Death Activator
Wing, J. P., Karres, J. S., Ogdahl, J. L., Zhou, L. J., Schwartz, L. M., & Nambu, J. R. (2002) · Current Biology · doi:10.1016/s0960-9822(01)00664-9 · Cited by 117 · see citing works
Laundrie, B., Peterson, J. S., Baum, J., Chang, J. C., Fileppo, D., Thompson, S. R., & McCall, K. (2003) · Genetics · doi:10.1093/genetics/165.4.1881 · Cited by 112 · see citing works
Beyond apoptosis: caspase regulatory mechanisms and functions in vivo
Kuranaga, E. (2012) · Genes to Cells · doi:10.1111/j.1365-2443.2011.01579.x · Cited by 111 · see citing works
Steroid regulation of programmed cell death during Drosophila development
Baehrecke, E. H. (2000) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400753 · Cited by 111 · see citing works
Stage-specific regulation of caspase activity in drosophila oogenesis
Peterson, J. S., Barkett, M., & McCall, K. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00240-9 · Cited by 110 · see citing works
Zhang, H., Huang, Q., Ning, K., Matsuyama, S., Hammock, B. D., Godzik, A., & Reed, J. C. (2000) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)61510-3 · Cited by 109 · see citing works
del Peso, L., González, V. M., & Núñez, G. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.50.33495 · Cited by 105 · see citing works
Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death
Orme, M. H., & Meier, P. (2009) · APOPTOSIS · doi:10.1007/s10495-009-0358-2 · Cited by 105 · see citing works
Autophagy occurs upstream or parallel to the apoptosome during histolytic cell death
Akdemir, F., Farkas, R., Chen, P., Juhász, G., Medved'ová, L., Sass, M., Wang, L., Wang, X., Chittaranjan, S., Gorski, S. M., et al. (2006) · Development · doi:10.1242/dev.02332 · Cited by 102 · see citing works
Patterning the fly eye: the role of apoptosis
Brachmann, C. B., & Cagan, R. L. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(02)00041-0 · Cited by 101 · see citing works
Kaplan, Y., Gibbs-Bar, L., Kalifa, Y., Feinstein-Rotkopf, Y., & Arama, E. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.06.009 · Cited by 99 · see citing works
Cakouros, D., Daish, T., Martin, D. N., Baehrecke, E. H., & Kumar, S. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200201034 · Cited by 99 · see citing works
Self-citationHuh, J. R., Foe, I. T., Muro, I., Chen, C., Seol, J. H., Yoo, S. J., Guo, M., Park, J. M., & Hay, B. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m608051200 · Cited by 97 · see citing works
Deterin, a New Inhibitor of Apoptosis from Drosophila melanogaster
Jones, G., Jones, D., Zhou, L., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000369200 · Cited by 95 · see citing works
Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster
Cavaliere, V., Taddei, C., & Gargiulo, G. (1998) · Development Genes and Evolution · doi:10.1007/s004270050160 · Cited by 93 · see citing works
Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1
Tenev, T., Zachariou, A., Wilson, R., Paul, A., & Meier, P. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf530 · Cited by 93 · see citing works
Cakouros, D., Daish, T., & Kumar, S. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200311057 · Cited by 93 · see citing works
Self-citationdDOR Is an EcR Coactivator that Forms a Feed-Forward Loop Connecting Insulin and Ecdysone Signaling
Francis, V. A., Zorzano, A., & Teleman, A. A. (2010) · Current Biology · doi:10.1016/j.cub.2010.08.055 · Cited by 92 · see citing works
Characterization of the DrosophilaCaspase, DAMM
Harvey, N. L., Daish, T., Mills, K., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009444200 · Cited by 91 · see citing works
Zhang, H., Huang, Q., Ning, K., et al. (2000) · PubMed · doi:10.1074/jbc.m002846200 · Cited by 89 · see citing works
Systematic in vivo RNAi analysis of putative components of the Drosophila cell death machinery
Leulier, F., Ribeiro, P. S., Palmer, E., Tenev, T., Takahashi, K., Robertson, D. M., Zachariou, A., Franck Pichaud, N., Ueda, R., & Meier, P. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401868 · Cited by 87 · see citing works
Programmed cell death and patterning in Drosophila
Rusconi, J. C., Hays, R. D., & Cagan, R. L. (2000) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400767 · Cited by 87 · see citing works
Baum, J., Arama, E., Steller, H., & McCall, K. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402155 · Cited by 82 · see citing works
Relationship between growth arrest and autophagy in midgut programmed cell death in Drosophila
Denton, D., Chang, T.-K., Nicolson, S., Shravage, B., Simin, R., Baehrecke, E. H., & Kumar, S. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2012.43 · Cited by 81 · see citing works
Self-citationStructure of the Drosophila Apoptosome at 6.9 Å Resolution
Yuan, S., Yu, X., Topf, M., Dorstyn, L., Kumar, S., Ludtke, S. J., & Akey, C. W. (2011) · Structure · doi:10.1016/j.str.2010.10.009 · Cited by 78 · see citing works
Self-citationDoumanis, J., Quinn, L. M., Richardson, H. E., et al. (2001) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400864 · Cited by 77 · see citing works
Mills, K., Daish, T., Harvey, K. F., Pfleger, C. M., Hariharan, I. K., & Kumar, S. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200512126 · Cited by 70 · see citing works
Self-citationThe Bax/Bak ortholog in Drosophila , Debcl, exerts limited control over programmed cell death
Galindo, K. A., Lu, W.-J., Park, J. H., & Abrams, J. (2008) · Development · doi:10.1242/dev.019042 · Cited by 68 · see citing works
Sevrioukov, E. A., Burr, J., Huang, E. W., Assi, H. H., Monserrate, J. P., Purves, D. C., Wu, J. N., Song, E. J., & Brachmann, C. B. (2007) · genesis · doi:10.1002/dvg.20279 · Cited by 67 · see citing works
Waldhuber, M., Emoto, K., & Petritsch, C. K. (2005) · Mechanisms of Development · doi:10.1016/j.mod.2005.04.003 · Cited by 67 · see citing works
del Peso, L., González, V. M., Inohara, N., Ellis, R. E., & Núñez, G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000858200 · Cited by 67 · see citing works
Wing, J. P., Schwartz, L. M., & Nambu, J. R. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00316-1 · Cited by 66 · see citing works
A biochemical analysis of the activation of the Drosophila caspase DRONC
Dorstyn, L., & Kumar, S. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402288 · Cited by 61 · see citing works
Self-citationKilpatrick, Z. E., Cakouros, D., & Kumar, S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413971200 · Cited by 60 · see citing works
Self-citationARK, the Apaf-1 related killer in Drosophila, requires diverse domains for its apoptotic activity
Srivastava, M., Scherr, H., Lackey, M., Xu, D., Chen, Z., Lu, J. T., & Bergmann, A. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401931 · Cited by 58 · see citing works
Lee, T. V., Fan, Y., Wang, S., Srivastava, M., Broemer, M., Meier, P., & Bergmann, A. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002261 · Cited by 57 · see citing works
Drosophila Omi, a mitochondrial‐localized IAP antagonist and proapoptotic serine protease
Challa-Malladi, M., Malladi, S., Pellock, B. J., Dresnek, D., Varadarajan, S., Yin, Y. W., White, K., & Bratton, S. B. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601745 · Cited by 57 · see citing works
Bax‐like protein Drob‐1 protects neurons from expanded polyglutamine‐induced toxicity in Drosophila
Senoo‐Matsuda, N., Igaki, T., & Miura, M. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600721 · Cited by 53 · see citing works
Conserved metabolic energy production pathways govern Eiger/TNF-induced nonapoptotic cell death
Kanda, H., Igaki, T., Okano, H., & Miura, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103242108 · Cited by 49 · see citing works
Lee, G., Wang, Z., Sehgal, R., Chen, C., Kikuno, K., Hay, B. A., & Park, J. H. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22498 · Cited by 46 · see citing works
Fork head controls the timing and tissue selectivity of steroid-induced developmental cell death
Cao, C., Liu, Y., & Lehmann, M. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200611155 · Cited by 45 · see citing works
A cytochrome c-free fly apoptosome
Dorstyn, L., & Kumar, S. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401918 · Cited by 43 · see citing works
Self-citationYin, V. P., Thummel, C. S., & Bashirullah, A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200703206 · Cited by 43 · see citing works
Evolution of mitochondrial cell death pathway: Proapoptotic role of HtrA2/Omi in Drosophila
Igaki, T., Suzuki, Y., Tokushige, N., Aonuma, H., Takahashi, R., & Miura, M. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.03.079 · Cited by 41 · see citing works
Cakouros, D., Daish, T., Mills, K., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400972200 · Cited by 38 · see citing works
Doumanis, J., Dorstyn, L., & Kumar, S. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402082 · Cited by 38 · see citing works
Self-citationEvolutionarily conserved Bok proteins in the Bcl‐2 family
Zhang, H., Holzgreve, W., & Geyter, C. D. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01921-9 · Cited by 38 · see citing works
Noncanonical cell death pathways act during Drosophila oogenesis
Peterson, J. S., Bass, B. P., Jue, D., Rodriguez, A., Abrams, J., & McCall, K. (2007) · genesis · doi:10.1002/dvg.20306 · Cited by 37 · see citing works
Distinct promoter regions regulate spatial and temporal expression of the Drosophila caspase dronc
Daish, T., Cakouros, D., & Kumar, S. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401312 · Cited by 32 · see citing works
Self-citationThe interaction of DIAP1 with dOmi/HtrA2 regulates cell death in Drosophila
Khan, F., Fujioka, M., Datta, P., Fernandes‐Alnemri, T., Jaynes, J. B., & Alnemri, E. S. (2008) · Cell Death and Differentiation · doi:10.1038/cdd.2008.19 · Cited by 29 · see citing works
Cakouros, D., Mills, K., Denton, D., Paterson, A., Daish, T., & Kumar, S. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200712169 · Cited by 29 · see citing works
Self-citationStructural mechanisms of DIAP1 auto-inhibition and DIAP1-mediated inhibition of drICE
Li, X., Wang, J., & Shi, Y. (2011) · Nature Communications · doi:10.1038/ncomms1418 · Cited by 29 · see citing works
grim promotes programmed cell death of Drosophila microchaete glial cells
Wu, J. N., Nguyen, N. T., Aghazarian, M., et al. (2010) · Mechanisms of Development · doi:10.1016/j.mod.2010.06.001 · Cited by 29 · see citing works
Genetic regulation of programmed cell death in Drosophila
Lee, C., & Baehrecke, E. H. (2000) · Cell Research · doi:10.1038/sj.cr.7290048 · Cited by 25 · see citing works
Drosophila Apoptosis and Bcl-2 Genes
Chen, P., & Abrams, J. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.148.4.625 · Cited by 19 · see citing works
Arama, E., Bader, M., Rieckhof, G. E., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050291 · Cited by 1 · see citing works
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Autophagy-dependent cell death
Denton, D., & Kumar, S. (2019) · Cell Death & Differentiation · doi:10.1038/s41418-018-0252-y · Cited by 777 · see citing works
Self-citationProgrammed cell death in aging
Tower, J. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.04.002 · Cited by 426 · see citing works
Distinct requirements of Autophagy-related genes in programmed cell death
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Self-citation
- Authors
- Denton, D., Aung-Htut, M. T., & Kumar, S.
- Affiliations
- South Australia Pathology (AU)
- Corresponding author
- Kumar, Sharad
- Venue
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 1833
- Issue
- 12
- Pages
- 3499-3506
- ISSN
- 0167-4889 (ISSN-L)
- OpenAlex
- W1990775733
- Cited by
- 75
- References
- 153
- Citations by year
- 2026: 1 · 2024: 5 · 2023: 8 · 2022: 7 · 2021: 8 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 6 · 2016: 6 · 2015: 11 · 2014: 6
- FWCI
- 0.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research (publishedVersion)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- National Health and Medical Research Council (NHMRC) (626903, 1041807)
- Senior Principal Research Fellowship (1002863)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- programmed cell death, Drosophila melanogaster, developmental cell death, cell death pathways, tissue patterning
- MeSH terms
- Animals, Drosophila melanogaster, Metamorphosis, Biological, Models, Biological, Signal Transduction, Apoptosis, Drosophila Proteins
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